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Signal processing in complex chemotaxis pathways

Key Points

  • Chemotaxis allows bacteria to swim towards environments that are better for growth. The process is involved in pathogenicity, biofilm formation and the establishment of symbiotic relationships.

  • Changes in attractant and repellent concentrations are detected by clusters of chemoreceptors. Bacteria can sense very small changes in attractant concentration over a wide range of background concentrations.

  • The chemoreceptor clusters control the activity of a two-component system comprising the histidine protein kinase CheA and the response regulators CheY and CheB. Phosphorylated CheY controls flagellar motor switching, whereas phosphorylated CheB mediates adaptation.

  • The Escherichia coli chemotaxis signalling pathway is one of the simplest and best understood, but it is becoming increasingly apparent that most bacteria have more complex chemosensory pathways involving multiple homologues of the E. coli chemotaxis proteins.

  • Rhodobacter sphaeroides has one of the best understood complex chemotaxis pathways; it has two distinct types of chemosensory cluster: one that is positioned at the cell pole and detects changes in the external attractant and repellent concentrations, and another that is cytoplasmic and is believed to monitor the metabolic state of the cell (a form of energy taxis).

  • Structural studies have revealed the specificity determinants in the interaction of CheY proteins with CheA proteins and allowed rewiring of the signalling pathway. Mechanisms of signal integration and signal termination have been elucidated by mathematical modelling.

  • Some bacteria have complex chemotaxis pathways that go beyond what is found in E. coli and R. sphaeroides. For example, in addition to the methylation-based adaptation system, Bacillus subtilis has two further adaptation pathways, one involving CheC and CheD and another using CheV.

  • Some bacteria exploit the ability of the chemotaxis circuitry to sense small changes in ligand concentrations, and use the system to control behaviour other than chemotaxis. For example, Myxococcus xanthus has a chemotaxis-like pathway controlling development of the fruiting body, and Pseudomonas aeruginosa has one controlling biofilm formation.

Abstract

Bacteria use chemotaxis to migrate towards environments that are better for growth. Chemoreceptors detect changes in attractant levels and signal through two-component systems to control swimming direction. This basic pathway is conserved across all chemotactic bacteria and archaea; however, recent work combining systems biology and genome sequencing has started to elucidate the additional complexity of the process in many bacterial species. This article focuses on one of the best understood complex networks, which is found in Rhodobacter sphaeroides and integrates sensory data about the external environment and the metabolic state of the cell to produce a balanced response at the flagellar motor.

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Figure 1: The Escherichia coli chemotaxis pathway.
Figure 2: The Rhodobacter sphaeroides chemotaxis pathways.
Figure 3: The two chemotaxis clusters of Rhodobacter sphaeroides.
Figure 4: The specificity of the CheA–CheY phosphotransfer, as revealed by the 1.4 Å resolution structure of the CheY6–CheA3P1 complex.
Figure 5: Alternative chemosensory pathways.

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Acknowledgements

This research was funded by the UK Biotechnology and Biological Sciences Research Council.

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Correspondence to Judith P. Armitage.

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Glossary

Two-component signalling pathway

A bacterial signalling system comprising histidine protein kinases and response regulators; these pathways regulate diverse processes, including virulence, development and chemotaxis.

Chemoeffector

A collective term for an attractant or repellent.

Histidine protein kinase

The sensor in a two-component signal transduction pathway. These kinases autophosphorylate at a conserved histidine residue using ATP as the phosphodonor. The rate at which they autophosphorylate is controlled by sensory stimuli. Following autophosphorylation, the kinase serves as a phosphodonor for a specific response regulator. CheA is the chemotaxis histidine protein kinase.

Response regulator

A protein containing a receiver domain that is phosphorylated on an aspartate residue by a histidine protein kinase. Phosphorylation of the receiver domain induces a conformational change that activates the response regulators. Signal termination is achieved by hydrolysis of the aspartyl-phosphate bond, catalysed by a phosphatase in some systems.

Autophosphorylation

The process in which a histidine protein kinase phosphorylates itself using ATP as the phosphodonor. Typically, the rate of this process is controlled by environmental stimuli.

Signal termination

The removal of the phosphoryl groups from the signalling pathway. This is achieved by hydrolysis of the aspartyl-phosphate bonds in the phosphorylated response regulators.

Adaptation

The process by which the signalling state of the chemotaxis pathway is reset to the background concentration of chemoeffectors experienced in the recent past. An adapted cell will have an intermediate tumble bias, allowing cells to respond either negatively or positively to future changes in chemoeffector concentration.

PAS domain

A domain named owing to its conservation in the protein families period circadian protein (PER), aryl hydrocarbon receptor nuclear translocator (ARNT) and single-minded (SIM). PAS domains bind a diverse range of small-molecule ligands (for example, haem and FAD) and are often involved in redox and light sensing.

Ordinary differential equation (ODE) mathematical model

As used here, a set of mathematical equations that represents the changes in the phosphorylation levels of the chemotaxis proteins as a function of time.

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Porter, S., Wadhams, G. & Armitage, J. Signal processing in complex chemotaxis pathways. Nat Rev Microbiol 9, 153–165 (2011). https://doi.org/10.1038/nrmicro2505

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